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Effects of goldfish (Carassius auratus) population size and body condition on the transmission of Gyrodactylus kobayashii (Monogenea)

Published online by Cambridge University Press:  15 May 2017

SHUN ZHOU ,
HONG ZOU ,
SHAN G. WU ,
GUI T. WANG ,
DAVID J. MARCOGLIESE  and
WEN X. LI
SHUN ZHOU
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China University of Chinese Academy of Sciences, Beijing 100049, P. R. China
HONG ZOU
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China
SHAN G. WU
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China
GUI T. WANG
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China
DAVID J. MARCOGLIESE
Affiliation:
Aquatic Contaminants Research Division, Water Science and Technology Directorate, Science and Technology Branch, Environment and Climate Change Canada, St. Lawrence Centre, 105 McGill, 7th floor, Montreal, QC H2Y 2E7, Canada
WEN X. LI*
Affiliation:
Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China
*
*Corresponding author: Key Laboratory of Aquaculture Disease Control, Ministry of Agriculture, and State Key Laboratory of Freshwater Ecology and Biotechnology, Institute of Hydrobiology, Chinese Academy of Sciences, Wuhan 430072, P. R. China. E-mail: liwx@ihb.ac.cn
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Summary

Field surveys indicate that host population size, rather than density, is the most important determinant of monogenean infection dynamics. To verify this prediction, epidemic parameters were monitored for 70 days at five host population sizes held at constant density using a goldfish – Gyrodactylus kobayashii laboratory model. During the first 20 days, the rate of increase of prevalence and mean abundance was faster in small host populations. Total mean prevalence and total mean abundance throughout the experiment were not significantly affected by host population sizes. Higher transmission rates were detected in larger host populations. However, there were no significant differences in effective contact rates among the five host populations on each sampling day during the first 20 days, implying that contact rates may be saturated at a sufficiently high host density. These results demonstrate that the epidemic occurs more quickly in smaller host populations at the beginning of the experiment. However, the epidemic is independent of the host population size due to the similar effective contact rates in the five population sizes. Significant negative influence of the initial body condition (Kn) of uninfected goldfish on total mean abundance of parasites suggests that susceptibility of hosts is also a determinant of parasite transmission.

Keywords

gyrodactylidstransmission dynamicsepidemicscontact ratedensity-dependant transmissionfrequency-dependant transmissionfish
Type
Research Article
Information
Parasitology , Volume 144 , Issue 9 , August 2017 , pp. 1221 - 1228
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Copyright
Copyright © Cambridge University Press 2017 

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Footnotes

†

Present address: St. Andrews Biological Station, Fisheries and Oceans Canada, 531 Brandy Cove Road, St. Andrews, New Brunswick E5B 2L9, Canada.

References

REFERENCES

Arneberg, P., Skorping, A., Grenfell, B. and Read, A. F. (1998). Host densities as determinants of abundance in parasite communities. Proceedings of the Royal Society B-Biological Sciences 265, 1283–1289.CrossRefGoogle Scholar
Bagge, A. M., Poulin, R. and Valtonen, E. T. (2004). Fish population size, and not density, as the determining factor of parasite infection: a case study. Parasitology 128, 305–313.CrossRefGoogle Scholar
Bakke, T. A., Harris, P. D., Jansen, P. A. and Hansen, L. P. (1992). Host specificity and dispersal strategy in gyrodactylid monogeneans, with particular reference to Gyrodactylus salaris (Platyhelminthes, Monogenea). Diseases of Aquatic Organisms 13, 63–74.Google Scholar
Bakke, T. A., Cable, J. and Harris, P. D. (2007). The biology of gyrodactylid monogeneans: the “Russian-doll killers”. Advances in Parasitology 64, 161–376.CrossRefGoogle Scholar
Barber, I., Hoare, D. and Krause, J. (2000). Effects of parasites on fish behaviour: a review and evolutionary perspective. Reviews in Fish Biology and Fisheries 10, 131–165.CrossRefGoogle Scholar
Beldomenico, P. M., Telfer, S., Gebert, S., Lukomski, L., Bennett, M. and Begon, M. (2008). Poor condition and infection: a vicious circle in natural populations. Proceedings of the Royal Society B-Biological Sciences 275, 1753–1759.CrossRefGoogle ScholarPubMed
Boeger, W. A., Kritsky, D. C., Pie, M. R. and Engers, K. B. (2005). Mode of transmission, host switching, and escape from the red queen by viviparous gyrodactylids (Monogenoidea). Journal of Parasitology 91, 1000–1007.Google Scholar
Bush, A. O., Lafferty, K. D., Lotz, J. M. and Shostak, A. W. (1997). Parasitology meets ecology on its own terms: Margolis, et al. revisited. Journal of Parasitology 83, 575–583.Google Scholar
Cable, J. and van Oosterhout, C. (2007). The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence. International Journal for Parasitology 37, 1449–1458.CrossRefGoogle ScholarPubMed
Cross, P. C., Cole, E. K., Dobson, A. P., Edwards, W. H., Hamlin, K. L., Luikart, G., Middleton, A. D., Scurlock, B. M. and White, P. J. (2010). Probable causes of increasing brucellosis in free-ranging elk of the Greater Yellowstone Ecosystem. Ecological Applications 20, 278–288.Google Scholar
Cross, P. C., Creech, T. G., Ebinger, M. R., Heisey, D. M., Irvine, K. M. and Creel, S. (2012). Wildlife contact analysis: emerging methods, questions, and challenges. Behavioral Ecology and Sociobiology 66, 1437–1447.Google Scholar
Cross, P. C., Creech, T. G., Ebinger, M. R., Manlove, K., Irvine, K., Henningsen, J., Rogerson, J., Scurlock, B. M. and Creel, S. (2013). Female elk contacts are neither frequency nor density dependent. Ecology 94, 2076–2086.CrossRefGoogle ScholarPubMed
Harris, P. D. (2011). Changes in the site specificity of Gyrodactylus turnbulli Harris, 1986 (Monogenea) during infections of individual guppies (Poecilia reticulata Peters, 1859). Canadian Journal of Zoology 66, 2854–2857.Google Scholar
Jackson, J. A. and Tinsley, R. C. (2001). Protopolystoma xenopodis (Monogenea) primary and secondary infections in Xenopus laevis . Parasitology 123, 455–463.CrossRefGoogle ScholarPubMed
Jansen, P. A. and Bakke, T. A. (2009). Temperature-dependent reproduction and survival of Gyrodactylus salaris Malmberg, 1957 (Platyhelminthes: Monogenea) on Atlantic salmon (Salmo salar L.). Parasitology 102, 105–112.Google Scholar
Johnson, M. B., Lafferty, K. D., van Oosterhout, C. and Cable, J. (2011). Parasite transmission in social interacting hosts: Monogenean epidemics in guppies. Plos ONE 6, e22634.CrossRefGoogle ScholarPubMed
Lecren, E. D. (1951). The length-weight relationship and seasonal cycle in gonad weight and condition in the perch (Perca fluviatilis). Journal of Animal Ecology 20, 201–219.Google Scholar
Leem, J. B., Jeon, W., Yun, C. Y. and Lee, S. H. (2012). Quantitative analysis of fish schooling behavior with different numbers of medaka (Oryzias latipes) and goldfish (Carassius auratus). Ocean Science Journal 47, 445–451.Google Scholar
Li, R., Li, W., Wu, X. and Wang, G. (2014). Identification of Gyrodactylus species in goldfish (Carassius auratus) through morphological study and the analysis of the rDNA ITS sequence. Acta Hydrobiologica Sinica 38, 903–909 (in Chinese).Google Scholar
Llewellyn, J. (1968). Larvae and larval development of monogeneans. Advances in Parasitology 6, 373–383.Google Scholar
Lloyd-Smith, J. O., Cross, P. C., Briggs, C. J., Daugherty, M., Getz, W. M., Latto, J., Sanchez, M. S., Smith, A. B. and Swei, A. (2005). Should we expect population thresholds for wildlife disease? Trends in Ecology & Evolution 20, 511–519.CrossRefGoogle ScholarPubMed
Marina, C. F., Fernandez-Salas, I., Ibarra, J. E., Arredondo-Jimenez, J. I., Valle, J. and Williams, T. (2005). Transmission dynamics of an iridescent virus in an experimental mosquito population: the role of host density. Ecological Entomology 30, 376–382.Google Scholar
McCallum, H., Barlow, N. and Hone, J. (2001). How should pathogen transmission be modelled? Trends in Ecology & Evolution 16, 295–300.CrossRefGoogle ScholarPubMed
Møller, A. P., Christe, P., Erritzoe, J. and Mavarez, J. (1998). Condition, disease and immune defence. Oikos 83, 301–306.Google Scholar
Olstad, K., Cable, J., Robertsen, G. and Bakke, T. A. (2006). Unpredicted transmission strategy of Gyrodactylus salaris (Monogenea: Gyrodactylidae): survival and infectivity of parasites on dead hosts. Parasitology 133, 33.Google Scholar
Peig, J. and Green, A. J. (2010). The paradigm of body condition: a critical reappraisal of current methods based on mass and length. Functional Ecology 24, 1323–1332.CrossRefGoogle Scholar
R Development Core Team (2014). R: a Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.Google Scholar
Ramsey, D., Spencer, N., Caley, P., Efford, M., Hansen, K., Lam, M. and Cooper, D. (2002). The effects of reducing population density on contact rates between brushtail possums: implications for transmission of bovine tuberculosis. Journal of Applied Ecology 39, 806–818.Google Scholar
Ryder, J. J., Miller, M. R., White, A., Knell, R. J. and Boots, M. (2007). Host-parasite population dynamics under combined frequency- and density-dependent transmission. Oikos 116, 2017–2026.CrossRefGoogle Scholar
Scott, M. E. and Anderson, R. M. (1984). The population dynamics of Gyrodactylus bullatarudis (Monogenea) within laboratory populations of the fish host Poecilia reticulata . Parasitology 89, 159–194.Google Scholar
Scott, M. E. and Nokes, D. J. (1984). Temperature-dependent reproduction and survival of Gyrodactylus bullatarudis (Monogenea) on guppies (Poecilia reticulata). Parasitology 89, 221–227.Google Scholar
Scott, M. E. and Smith, G. (1994). Parasitic and Infectious Diseases: Epidemiology and Ecology. Academic Press, San Diego, USA.Google Scholar
Smith, K. F., Acevedo-Whitehouse, K. and Pedersen, A. B. (2009 a). The role of infectious diseases in biological conservation. Animal Conservation 12, 1–12.Google Scholar
Smith, M. J., Telfer, S., Kallio, E. R., Burthe, S., Cook, A. R., Lambin, X. and Begon, M. (2009 b). Host-pathogen time series data in wildlife support a transmission function between density and frequency dependence. Proceedings of the National Academy of Sciences of the United States of America 106, 7905–7909.Google Scholar
Stringer, A. P. and Linklater, W. L. (2015). Host density drives macroparasite abundance across populations of a critically endangered megaherbivore. Oecologia 179, 201–207.CrossRefGoogle ScholarPubMed
Tadiri, C. P., Dargent, F. and Scott, M. E. (2013). Relative host body condition and food availability influence epidemic dynamics: a Poecilia reticulata-Gyrodactylus turnbulli host-parasite model. Parasitology 140, 343–351.CrossRefGoogle ScholarPubMed
Tinsley, R. C. and Jackson, J. A. (2002). Host factors limiting monogenean infections: a case study. International Journal for Parasitology 32, 353–365.Google Scholar
Warburton, E. M., Pearl, C. A. and Vonhof, M. J. (2016). Relationships between host body condition and immunocompetence, not host sex, best predict parasite burden in a bat-helminth system. Parasitology Research 115, 2155–2164.Google Scholar
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